Academic journal article Cognitive, Affective and Behavioral Neuroscience

When Is an Error Not a Prediction Error? an Electrophysiological Investigation

Academic journal article Cognitive, Affective and Behavioral Neuroscience

When Is an Error Not a Prediction Error? an Electrophysiological Investigation

Article excerpt

A recent theory holds that the anterior cingulate cortex (ACC) uses reinforcement learning signals conveyed by the midbrain dopamine system to facilitate flexible action selection. According to this position, the impact of reward prediction error signals on ACC modulates the amplitude of a component of the event-related brain potential called the error-related negativity (ERN). The theory predicts that ERN amplitude is monotonically related to the expectedness of the event: It is larger for unexpected outcomes than for expected outcomes. However, a recent failure to confirm this prediction has called the theory into question. In the present article, we investigated this discrepancy in three trial-and-error learning experiments. All three experiments provided support for the theory, but the effect sizes were largest when an optimal response strategy could actually be learned. This observation suggests that ACC utilizes dopamine reward prediction error signals for adaptive decision making when the optimal behavior is, in fact, learnable.

The anterior cingulate cortex (ACC) constitutes a central component of a neural system for cognitive control (Ridderinkhof, Ullsperger, Crone, & Nieuwenhuis, 2004). Theories about ACC function alternatively hold that it is responsible for detecting response conflict (Botvinick, Braver, Barch, Carter, & Cohen, 2001) or for the adaptive modification of behavior by relating actions with their consequences (Holroyd & Coles, 2002, 2008; Rushworth, Walton, Kennerley, & Bannerman, 2004). Notably, a recent theory holds that ACC uses reinforcement learning signals conveyed by the midbrain dopamine system to update the response selection process (Holroyd & Coles, 2002). This theory proposes that the impact of these dopamine signals on the ACC modulates the amplitude of a component of the event-related brain potential (ERP) called the errorrelated negativity (ERN). The ERN appears to exist in at least two forms: The "response ERN" (rERN) reflects a difference in neural processing between error responses and correct responses in speeded response time (RT) tasks (Falkenstein, Hohnsbein, Hoormann, & Blanke, 1990; Gehring, Goss, Coles, Meyer, & Donchin, 1993), and the "feedback ERN" (fERN) reflects a difference in neural processing between error feedback and correct feedback in guessing and trial-and-error learning tasks (Holroyd & Krigolson, 2007; Miltner, Braun, & Coles, 1997; for reviews, see Holroyd, Nieuwenhuis, Mars, & Coles, 2004; Nieuwenhuis, Holroyd, Mol, & Coles, 2004). Furthermore, experiments in the monkey have demonstrated that the midbrain dopamine system carries "reward prediction error signals"; phasic increases and decreases from baseline firing rate follow unexpected rewards and absences of reward, respectively (Schultz, 2002), which are then used by the targets of the dopamine system for the purpose of reinforcement learning (Montague, Hyman, & Cohen, 2004). Because of this property, the dopamine/ ERN theory- sometimes called the reinforcement learning theory of the ERN, or RL-ERN theory-predicts that fERN amplitude should be monotonically related to the unexpectedness of the outcome: When measured as the difference between the ERPs associated with correct and error trials, relatively large fERNs will be elicited by unexpected outcomes, whereas relatively small fERNs will be elicited by expected outcomes (Holroyd & Coles, 2002; Holroyd & Krigolson, 2007; see also Holroyd, Pakzad- Vaezi, & Krigolson, 2008).

There is now a great deal of evidence that the ERN indexes a reward prediction error signal (Baker & Holroyd, in press; Butterfield & Mangels, 2003; Cohen & Ranganath, 2007; Compton et al., 2007; Donkers & van Boxtel, 2005; Dunning & Hajcak, 2007; Eppinger, Kray, Mock, & Mecklinger, 2008; Hajcak, Moser, Holroyd, & Simons, 2007; Hewig et al., 2007, 2008; Holroyd & Coles, 2002, 2008; Holroyd & Krigolson, 2007; Holroyd, Nieuwenhuis, Yeung, & Cohen, 2003; Krigolson & Holroyd, 2007; Krigolson, Mathewson, Baker, Baker, & Holroyd, 2006; Krigolson, Pierce, Holroyd, & Tanaka, in press; Morris, Heerey, Gold, & Holroyd, 2008; Nieuwenhuis, Nielen, Mol, Hajcak, & Veltman, 2005; Nieuwenhuis et al. …

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